ACTA ZOOLOGICA BULGARICA Research Article Acta zool. bulg., Suppl. 10, 2017: 115-120

Confiscated orbicularis (L., 1758) Dying Out in a “Temporary” Reception Facility in Serbia: a Case Study Showing the Urgency for a Regional Rescue Centre

Sonja Nikolić1,2& Ana Golubović1,2

1Institute of Zoology, Faculty of Biology, University of Belgrade, Studentski trg 16, 11000 Belgrade, Serbia; E-mails: [email protected], [email protected] 2Serbian Herpetological Society “Milutin Radovanović”, Bulevar despota Stefana 142, 11000 Belgrade, Serbia; E-mail: [email protected]

Abstract: In December 2012, an illegal shipment of over 1,300 live European Pond (Emys orbicularis) was confiscated at the border between the Former Yugoslav Republic of Macedonia (FYROM) and Serbia. All were housed in the Belgrade Zoo, Serbia, as a temporary measure until officials of the two countries find a way to return them to their place of origin. Turtles were placed in an enclosure of c. 300 m2 with an artificial pond c. 1.3 m deep, where some European Pond Turtles and several exotic Red-eared Sliders have already been kept. Along with imposing intense stress, these circumstances are ideal for transmission of pathogens. In December 2017, the turtles are still in the zoo, with officials not having taken proactive measures. As a result of poor living conditions, many of these turtles died, and many suffer from various diseases and disorders. Therefore, they cannot be released anywhere into nature. The case we describe highlights the urgency of establishing multi-level national and regional cooperation, and one or more centres where confiscated animals and unwanted pets could be accepted and processed. Another important measure is the development of a range-wide DNA database of reptile threatened with illegal collection and trade. In future, the proposed conservation measures could enable timely returns of such animals into their source populations.

Key words: European Pond , Balkan Peninsula, illegal trade, inadequate housing, pathology, impossible release/ return to nature

Introduction Illegal wildlife trade is “the second largest illegal species has been facilitated through the trade in the world“ (Zimmerman 2003). In general, Internet (e.g. Mărginean & Gherman 2015). the rarer is the species, the higher is its price on the Throughout the Balkans, several chelonian spe- black market. Among chelonians, at least two ex- cies are targeted by illegal collectors (both for indi- tremely rare and critically endangered species are vidual use and for commercial operations) although, under severe illegal trade pressure, reaching prices like in other European countries, many of them are of 60,000 USD per individual as for yni- protected by law (e.g. in Serbia, see Anonymous phora, the rarest chelonian in the world (Leuteritz 2010a, b). In previous years, much has been done & Pedrono 2008, Kiester et al. 2013) and for concerning the education of regular and border po- leytensis (Asian Turtle Trade lice and customs officers, wildlife inspectors and ju- Working Group 2000, Madagascar Research dicature in Serbia (e.g. Ajtić et al. 2011). These ef- and Conservation Institute 2016, TRAFFIC forts resulted in increased number of confiscations of 2015b). In the past decades, illegal trade in various chelonians and various other animals. Nevertheless,

115 Nikolić S. & A. Golubović the level of knowledge is still very low regarding females and 109 juveniles. They were all placed in a protected species and biodiversity in general among shallow artificial pool (up to 1.3–1.5 m deep) where officials, judicature and in the general public. 30–50 European Pond Turtles of unknown origin Irrespective of formal protection, the have already been kept, along with several Red- European Pond Turtle, Emys orbicularis (L., 1758) eared Sliders ( scripta elegans). The en- (Testudines: ) is occasionally illegally tire enclosure where all these turtles were held (Fig. harvested from the wild in many parts of its range 1a) is smaller than 300 m2: this resulted in extremely (e.g. Velo-Antón et al. 2008). Its international con- high density of at least 4.5 ind./m2 (Fig. 1b). This servation status is “Lower Risk / Near Threatened”, calculated density is far above those noted in natural largely due to wide distribution range; however, this populations (Cadi et al. 2004, Balázs & Györffy IUCN assessment is from 20 years ago ( 2006) being about six ind./300 m2. A little central and Freshwater Turtle Specialist Group 2016). island exists in the pool, and along the shores there is In numerous European countries, E. orbicularis is certain amount of soil/gravel and reeds (suitable for highly threatened and recognised as critically en- basking, hiding, and for egg laying); several small dangered or even locally extinct (Fritz & Chiari logs near the reeds are also used for basking. There 2013, Jablonski et al. 2015). Extensive efforts and are also captive and wild aquatic birds, which can resources are devoted to its conservation (Velo- freely visit and leave the pond (this space was pri- Antón et al. 2008, Ayres et al. 2013, Mollov et al. marily intended for birds). In July 2014 (one and a 2013, Canessa et al. 2016). These issues were ad- half years after the confiscation), by the of the dressed in detail in the 2015 symposium devoted to Ministry of agriculture and nature conservation of E. orbicularis and other European freshwater turtles Serbia, the authors checked the state of the turtles (Fritz et al. 2017). In Serbia, the European Pond and took blood and tissue samples of live and dead Turtle is strictly protected (Anonymous 2010b), individuals. but it is still Data Deficient and of Least Concern (Krizmanić & Džukić 2015). Even basic informa- tion, such as precise data on its current distribution, Results and Discussion were only recently published (Krizmanić et al. By July 2014, the zoo employees had found 105 car- 2015) and further updated (Golubović et al. 2017). casses of E. orbicularis in the enclosure. There is a In the present article, we describe a case of legal probability that more dead animals were not found, rescue measures undertaken by the relevant authori- being burrowed or sunken. The carcasses were kept ties of the Republic of Serbia after the confiscation in a cooler until further processing (Fig. 2): per lo- of an illegal shipment of over 1,300 European Pond cal law, dead animals from confiscations must be Turtles at the border between the Former Yugoslav checked, counted and officially written off before Republic of Macedonia and Serbia. The analysis of being eliminated. this case elucidates the inadequate level of prepara- The Ministry of Agriculture and Nature tion for solving such cases demonstrated by both Conservation of Serbia has signed contracts with state authorities and research community at the na- two zoos in Serbia (in Belgrade and Palić) for tem- tional and international levels. porary acceptance and caring for the animals con- fiscated on Serbian borders. The zoos must accept confiscated animals, and the Ministry is obliged to Materials and Methods provide subsistence for these animals if they are not In December 2012, on the border between FYROM publicly exhibited (Serbian CITES office, pers. and Serbia, 1,327 individuals of E. orbicularis were comm.). The zoos (which often face difficulties with confiscated, and taken to the Belgrade Zoo, to be basic, day-to-day financing and maintenance) devote housed “temporarily” (Serbian CITES office, pers. serious efforts to respond to such a difficult task. For comm.). The suspect for this smuggling attempt es- the seized animals they must provide adequate con- caped, before the authorities could obtain informa- ditions: space, food, temperature, humidity, condi- tion on the origin of turtles. According to expert tions for hibernation, etc. All this is, however, some- opinion, the animals could have originated from times not possible. Often no real quarantine is pro- natural habitats in FYROM, Albania and (or) Greece vided, and animals from various sources are housed (Serbian CITES office, pers. comm.). Serbian sci- together, often for long periods, like in our case. entific authority (herpetologist of the Institute for One of serious complications which emerge Nature Conservation of Serbia) identified, counted from suboptimal housing is that animals can ex- and sexed the animals: there were 674 males, 544 change diseases and parasites, and they can

116 Confiscated Emys orbicularis (L., 1758) Dying Out in a “Temporary” Reception Facility in Serbia...

Fig. 1. (a) Part of the enclosure with turtles (picture taken on 22 February 2016, by S. N.); (b) high density of E. orbicularis on the shore (picture taken on 2 March 2014 by A. G.) interbreed. These interactions “contaminate” ani- mals in more than one way, and preclude their return into nature, even if their source population is known (i.e. confessed by the offenders). In cases of illegal collection of animals from the wild, such “contami- nation” problems probably start some time before shipping, given that animals have to be kept in some kind of enclosure until a satisfactory number is col- lected, often from several localities/populations. In the concrete case, the animals were transported in December, when they should be hibernating: their collecting from nature must have occurred several months earlier. Approximately a year and a half after the con- Fig. 2. Dead E. orbicularis from the freezer in the zoo fiscation of turtles, the zoo veterinarian and his col- (picture taken on 18 February 2014 by A. G.) leagues found a number of diseases and other disor- ders in these animals: mycoses, bacterial and viral infections, ecto- and endoparasites, necroses, anae- Until the time of final preparation of this manu- mia, complications with internal organs (Özvegy script (December 2017, five years after the confisca- et al. 2015, Özvegy 2016). Also, they noted in- tion) no solution was found for these turtles: they are festation of all sampled individuals (n = 30) with still in the zoo and there are no attempts at solving Haemogregarina stepanowi (Özvegy et al. 2015, the problem. The authors have not repeated the visit Özvegy 2016). It is impossible to determine if the to the enclosure with turtles, and no precise informa- parasite came with the confiscated animals, or it tion exists on their current state. was previously present in the captive turtles. The The problem of illegal wildlife trade is neither observed parasites and other maladies are present unique nor uncommon in the Balkans, but is not in natural turtle populations, including E. orbicula- easily documented. Actually, even in the European ris (e.g. Dvořákova et al. 2013) but at lower inci- Union and even for the CITES-listed species it is dences. In Serbia, such investigations have not been often hard to obtain precise data on illegal wild- performed before the study undertaken by Özvegy life trade with other parts of the world. For exam- et al. (2015). Their results confirmed our concerns ple, in 2013 and 2014, and their parts/de- regarding risks of keeping too many individuals un- rivatives comprised 19% and 18%, respectively, of der inadequate conditions. By the opinion of veteri- “important individual seizures reported by Member narians and colleague biologists, E. orbicularis indi- States” (TRAFFIC 2014, 2015a). The numbers of viduals cannot be released from the Belgrade Zoo in unreported and “unimportant” incidents remain un- the given state. known.

117 Nikolić S. & A. Golubović

Because illegal trade with wild animals is flour- if any health problem is detected, i.e. if captive or ishing, we expect that in future more confiscations confiscated animals are found positive for any dis- will be made on Serbian borders. This means higher ease or increased load of (usually naturally present) demands for resources for adequate care and treat- parasites, they should not be taken anywhere to na- ment of those animals. The problem of housing con- ture. Such projects are not impossible, but are time- fiscated animals could be resolved if more space was and resources-consuming. Also, they imply constant provided for/in the zoos, and if acceptance programs involvement of experts from many fields (phyloge- were permanently financed by state authorities. ography, ecology, veterinary medicine; national and Proper quarantine and health screening are costly international law, etc.), from all countries covered by in terms of both money and space, and sometimes species ranges. A core of the best practices suggested are simply not possible. Also, interest about wildlife in such occasions are summarized in “the Kiten pro- crime is often not among the state priorities. tocol” (Kornilev et al. 2017). Tragically, the number of individuals confiscat- During the past few years, we made the first ed in our example is 2/3 the total number of captive- steps in Serbia. We managed to update distributional bred E. orbicularis (ca. 900) released into natural or data and to collect tissue samples of E. orbicularis restored habitats during costly reintroduction projects (and of some other species) from numerous wild in Germany, Spain, Czech Republic and other coun- populations. In future we must focus on DNA analy- tries, during several decades. This number was ob- ses and further population studies of wild European tained from seven studies, covering much of Europe Pond Turtle populations, and on establishing coop- (Mascort & Budó 2017, Meeske 2015, Ottonello et eration with colleagues from other, primarily Balkan al. 2015, Poggenburg et al. 2015, Pupins et al. 2015, countries inhabited by E. orbicularis. Only an inte- Schneeweiss & Beckmann 2015, Šebela 2017). grated approach can provide long-term persistence Preferably, a regional centre should be built, of this threatened species, which has already gone where confiscated animals and unwanted (native or extinct in certain parts of its range. exotic) pets could be housed and cared for. However, a severe problem remains: what is to be done with confiscated animals? They cannot be kept in zoos/ Acknowledgements: Field investigations of chelonians in Ser- bia were financed by the Rufford Foundation (Grants No. 16922- centres in unlimited numbers for long periods of time, 2 and 12291-1).The Ministry of energetics, development and na- nor can be released “somewhere” in a natural habitat ture conservation of the Republic of Serbia and its CITES office in some Balkan or European country. Illustrative of provided the means for collecting DNA samples from reptiles this problem is the case of over a 1,000 individuals threatened with illegal activities (No. 401-00-002432014-08); of hermanni confiscated on the border from we obtained the permission for collecting their tissue samples (No. 353-01-640/2014-08). For sampling E. orbicularis from Serbia to Hungary in 2014, which were “returned” wild populations, the permission from the Ministry of agri- to Bulgaria – after DNA analyses, with no consulta- culture and nature conservation of the Republic of Serbia was tion with Serbian experts (Hungarian CITES of- obtained (119-01-13-2-2015-09). The zoo veterinarian, Jòzsef fice). The animals must not be released (returned) Özvegy, provided us access to the enclosure, information about into nature without precise knowledge of their origin conditions in the enclosure and diseases in turtles, and help with tissue sampling of turtles. Biology students and colleagues, and through a wide-range study of DNA profiles of natu- members of the Serbian Herpetological Society participated in ral populations. Ideally, the entire distribution ranges fieldwork. Two anonymous reviewers helped us improve the of the threatened species should be covered. Also, manuscript.

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Accepted: 22.11.2017

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